Extreme soil adaptations

Some of the most remarkable adaptations in plants include adaptation to extreme edaphic stress. Therefore we are applying genome scanning approaches to understand the solutions evolution offers in some of the many independently-evolved lineages of metal, drought, and serpentine-tolerant plants. Our initial results point to broadly orchestrated, polygenic responses to these selective pressures. Concerted changes indicate that even in the case of an environmetnal pressure, well-orchestrated internal adaptations may be marshalled, calling for a better understanding of internal adaptation (i.e., systems-based analysis of compensatory changes in the genome). In addition, these first results are pointing to striking instances of repeated evolution and gene flow between species that may mediate some of these adaptations.

Why Serpentine?

Serpentine soils present a multidimensional hazard to plant life. Not only do they offer marginal levels of essential nutrients such as Ca, P, K, and N, but they are also usually very porous, with a high propensity toward drought. Low Ca:Mg ratios are a defining feature of serpentine environments and result in very low Ca uptake. These insults are typically compounded by the presence of phytotoxic levels of heavy metals such as Ni, Cd, and Zn, which leads to stunting and chlorosis, along with antagonistic effects on Fe uptake. As a result, serpentine environments are characterized by minimal ecosystem productivity and high rates of endemism. Evolution has nevertheless forged populations that thrive among these stresses, which by adapting to this ‘serpentine syndrome,’ suggest solutions to challenges in crop improvement.

In contrast to our recent work on adaptation to genome duplication in the same A. arenosa system, we discovered a relatively diverse array of genes implicated in serpentine adaptation, from strong sweeps in dehydration tolerance coding loci (ERD4 below), to loci involved in sulfur transport (SULTR1;1), metal transport, and root growth. We see clear selective sweeps in many categories consistent with adaptation to ‘serpentine syndrome’: dehydration tolerance, ion transport (Ca, Mg, and K transport-related genes), stress, and root branching and growth.

Figure below: selective sweeps on A. lyrata alleles in serpentine A. arenosa. (A) Allele frequency differences in two example differentiated regions. Dots represent single polymorphic SNPs. X-axis gives chromosome location. Y-axis gives degree of differentiation calculated by plotting the difference in allele frequencies between serpentine and non-serpentine populations. Arrows indicate gene models. Black arrow indicates sweep candidate with localized differentiation. (B) Linear plot showing the proportion of SNPs shared between the three pairwise populations comparisons in the same region as in (4A). (C) Sequence similarity at the same regions amongst A. lyrata, Gulsen (Serpentine A. arenosa), and Kasparstein (Non-serpentine A. arenosa) visualized using a RBG color triangle. Areas where two rows show the same colour (yellow) indicate localized high similarity specifically between Gulsen and A. lyrata, but not other nearby A. arenosa populations. These two lyrata-like alleles exhibit some of the highest Fst, 2dSFS CLR, and other selective sweep metric levels in the genome, specifically in the serpentine-adapted A. arenosa population.

In recent genome scans we see many such clear signatures of selection, typically consisting of single gene peaks of high differentiation, falling off immediately flanking gene coding loci, due to negligible linkage in A. arenosa. This makes identification of candidate genes unambiguous. Happily, most of our top selective sweep candidates have serpentine-relevant adaptive functions (from published studies, not simply GO assignments): e.g., dehydration tolerance genes, heavy metal transporters, and root macronutrient uptake transporters. This provides a rich set of candidate genes for upcoming functional analysis of alternate natural alleles mediating the striking adaptations we see in these remarkable plants.

We interpret these results as showing us not only adaptations to external challenges, but also compensatory adjustments to the changed physiological state of the cell. The work above is part of a set of ongoing collaborations with David Salt (Nottingham, U.K.).